Abstract
Natural olfactory stimuli are often complex mixtures of volatiles, of which the identities and ratios of constituents are important for odor-mediated behaviors. Despite this importance, the mechanism by which the olfactory system processes this complex information remains an area of active study. In this review, we describe recent progress in how odorants and mixtures are processed in the brain of insects. We use a comparative approach toward contrasting olfactory coding and the behavioral efficacy of mixtures in different insect species, and organize these topics around four sections: (1) Examples of the behavioral efficacy of odor mixtures and the olfactory environment; (2) mixture processing in the periphery; (3) mixture coding in the antennal lobe; and (4) evolutionary implications and adaptations for olfactory processing. We also include pertinent background information about the processing of individual odorants and comparative differences in wiring and anatomy, as these topics have been richly investigated and inform the processing of mixtures in the insect olfactory system. Finally, we describe exciting studies that have begun to elucidate the role of the processing of complex olfactory information in evolution and speciation.
Similar content being viewed by others
Abbreviations
- AL:
-
Antennal lobe
- AN:
-
Antennal nerve
- GABA:
-
γ-Aminobutyric acid
- LH:
-
Lateral horn of the protocerebrum
- LN:
-
Local interneuron
- eLN:
-
Excitatory local interneuron
- iLN:
-
Inhibitory local interneuron
- MB:
-
Mushroom bodies
- MGC:
-
Macroglomerular complex
- OB:
-
Olfactory bulb
- OR:
-
Olfactory receptor
- OBP:
-
Odorant binding protein
- ORC:
-
Olfactory receptor cell
- PN:
-
Projection neuron
References
Acebes A, Martin-Pena A, Chevalier V, Ferrus A (2011) Synapse loss in olfactory local interneurons modifies perception. J Neurosci 31:2734–2745
Andersson MN, Larsson MC, Blazenec M, Jakus R, Zhang Q-H, Schlyter F (2010) Peripheral modulation of pheromone response by inhibitory host compound in a beetle. J Exp Biol 213:3332–3339
Anton S, Homberg U (1999) Antennal lobe structure. In: Hansson B (ed) Insect olfaction. Springer, Berlin, pp 97–124
Anton S, Ignell R, Hansson BS (2002) Developmental changes in the structure and function of the central olfactory system in gregarious and solitary desert locusts. Microsc Res Tech 56:281–291
Assisi C, Stopfer M, Bazhenov M (2012) Excitatory local interneurons enhance tuning of sensory information. PLoS Comp Biol 8:e1002563
Ayasse M, Schiestl FP, Paulus HF, Löfstedt C, Hansson B, Ibarra F, Francke W (2000) Evolution of reproductive strategies in the sexually deceptive orchid Ophrys sphegodes: how does flower-specific variation of odor signals influence reproductive success? Evolution 54:1995–2006
Baker TC (2008) Balanced olfactory antagonism as a concept for understanding evolutionary shifts in moth sex pheromone blends. J Chem Ecol 34:971–981
Bargmann CI (2006) Comparative chemosensation from receptors to ecology. Nature 444:295–301
Barrozo RB, Jarriault D, Simeone X, Gaertner C, Gadenne C, Anton S (2010) Mating-induced transient inhibition of responses to sex pheromone in a male moth is not mediated by octopamine or serotonin. J Exp Biol 213:1100–1106
Bartelt RJ, Schaner AM, Jackson LL (1985) Cis-vaccenyl acetate as an aggregation pheromone in Drosophila melanogaster. J Chem Ecol 11:1747–1756
Behmer ST, Belt CE, Shapiro MS (2005) Variable rewards and discrimination ability in an insect herbivore: what and how does a hungry locust learn? J Exp Biol 208:3463–3473
Benton R (2006) On the origin of smell: odorant receptors in insects. Cell Mol Life Sci 63:1579–1585
Benton R, Sachse S, Michnick SW, Vosshall LB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4:240–257
Bhandawat V, Olsen SR, Gouwens NW, Schlief ML, Wilson RI (2007) Sensory processing in the Drosophila antennal lobe increases the reliability and separability of ensemble odor representations. Nat Neurosci 10:1474–1482
Bleeker MAK, Smid HM, Steidle JLM, Kruidhof HM, Van Loon JJA (2006) Differences in memory dynamics between two closely related parasitoid wasp species. Anim Behav 71:1343–1350
Brill MF, Rosenbaum T, Reus I, Kleineidam CJ, Nawrot MP, Rössler W (2013) Parallel processing via a dual olfactory pathway in the honeybee. J Neurosci 33:2443–2456
Carcaud J, Hill T, Giurfa M, Sandoz J-C (2012) Differential coding by two olfactory subsystems in the honeybee brain. J Neurophysiol 108:1106–1121
Carey AF, Carlson JR (2011) Insect olfaction from model systems to disease control. Proc Nat Acad Sci USA 108:12987–12995
Carr W, Derby CD (1986) Chemically stimulated feeding-behavior in marine animals—importance of chemical-mixtures and involvement of mixture interactions. J Chem Ecol 12:989–1011
Chaffiol A, Kropf J, Barroxo RB, Gadenne C, Rospars J-P, Anton S (2012) Plant odour stimuli reshape pheromonal representation in neurons of the antennal lobe macroglomerular complex of a male moth. J Exp Biol 215:1670–1680
Chittka L, Raine NE (2006) Recognition of flowers by pollinators. Curr Opin Plant Biol 9:428–435
Chou YH, Spletter ML, Yaksi E, Leong JC, Wilson RI, Luo L (2010) Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nat Neurosci 13:439–449
Choudhary AF, Laycock I, Wright GA (2012) Gamma-aminobutyric acid receptor A-mediated inhibition in the honeybee’s antennal lobe is necessary for the formation of configural olfactory percepts. Eur J Neurosci 35:1718–1724
Christensen TA, Mustaparta H, Hildebrand JG (1989) Discrimination of sex pheromone blends in the olfactory system of the moth. Chem Senses 14(3):463–477
Christensen TA, Mustaparta H, Hildebrand JG (1991) Chemical communication in heliothine moths 2. Central processing of intraspecific and interspecific olfactory message in the male corn-earworm Helicoverpa zea. J Comp Physiol A 169:259–274
Christensen TA, Lei H, Hildebrand JG (2003) Coordination of central odor representations through transient non-oscillatory synchronization of glomerular output neurons. Proc Nat Acad Sci USA 100:11076–11081
Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland
Dacks AM, Nighorn AJ (2011) The organization of the antennal lobe correlates not only with phylogenetic relationship, but also life history: a basal hymenopteran as exemplar. Chem Senses 36:209–220
Dacks AM, Christensen TA, Hildebrand JG (2008) Modulation of olfactory information processing in the antennal lobe of Manduca sexta. J Neurophysiol 99:2077–2085
Dacks AM, Riffell JA, Martin JP, Gage SL, Nighorn AJ (2012) Olfactory modulation by dopamine in the context of aversive learning. J Neurophysiol 108:539–550
Daly KC, Christensen TA, Lei H, Smith BH, Hildebrand JG (2004) Learning modulates the ensemble representations for odors in primary olfactory networks. Proc Natl Acad Sci USA 101:10476–10481
Daniel PC, Derby CD (1991) Mixture suppression in behavior—the antennular flick response in the spiny lobster towards binary odorant mixtures. Physiol Behav 49:591–601
de Bruyne M, Baker TC (2008) Odor detection in insects: volatile codes. J Chem Ecol 34:882–897
de Bruyne M, Foster K, Carlson JF (2001) Odor coding in the Drosophila antenna. Neuron 30:537–552
Deisig N, Lachnit H, Giurfa M (2002) The effect of similarity between elemental stimuli and compounds in olfactory patterning discriminations. Learn Memory 9:112–121
Deisig N, Giurfa M, Lachnit H, Sandoz JC (2006) Neural representation of olfactory mixtures in the honeybee antennal lobe. Eur J Neurosci 24(4):1161–1174
Deisig N, Giurfa M, Sandoz JC (2010) Antennal lobe processing increases separability of odor mixture representations in the honeybee. J Neurophysiol 103(4):2185–2194
Deisig N, Kropf J, Vitecek S, Pevergne D, Rouyar A, Sandoz J-C, Lucas P, Gadenne C, Anton S, Barrozo R (2012) Differential interactions of sex pheromone and plant odour in the olfactory pathway of a male moth. PLoS ONE 7:e33159
Dekker T, Steib B, Carde RT, Geier M (2002) l-lactic acid: a human-signifying host cue for the anthropophilic mosquito Anopheles gambiae. Med Vet Entomol 16:91–98
Dekker T, Ibba I, Siju KP, Stensymyr MC, Hansson BS (2006) Olfactory shifts parallel superspecialism for toxic fruit in Drosophila melanogaster sibling. D. sechellia. Curr Biol 16:101–109
Derby CD (2000) Learning from spiny lobsters about chemosensory coding of mixtures. Physiol Behav 69:203–209
Derby CD, Hamilton KA, Ache BW (1984) Processing of olfactory information at 3 neuronal levels in the spiny lobster. Brain Res 300:311–319
Derby CD, Ache BW, Kennel EW (1985) Mixture suppression in olfaction—electrophysiological evaluation of the contribution of peripheral and central neural components. Chem Senses 10:301–316
Derby CD, Girardot MN, Daniel PC (1991a) Responses of olfactory receptor cells of spiny lobsters to binary mixtures. 1. Intensity mixture interactions. J Neurophysiol 66:112–130
Derby CD, Girardot MN, Daniel PC (1991b) Responses of olfactory receptor cells of spiny lobsters to binary mixtures. 2. Pattern mixture interactions. J Neurophysiol 66:131–139
Ejima A, Smith BPC, Lucas C, Van Naters WV, Miller CJ, Carlson JR, Levine JD, Griffith LC (2007) Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Curr Biol 17:599–605
Ellen CW, Mercer AR (2012) Modulatory actions of dopamine and serotonin on insect antennal lobe neurons: insights from studies in vitro. J Mol Histol 43:401–404
El-Sayed AM (2012) The pherobase: database of pheromones and semiochemicals. http://www.pherobase.com
Eschbach C, Vogt K, Schmuker M, Gerber B (2011) The similarity between odors and their binary mixtures in Drosophila. Chem Senses 36:613–621
Farine JP, Legal L, Moreteau B, LeQuere JL (1996) Volatile components of ripe fruits of Morinda citrifolia and their effects on Drosophila. Phytochem 41:433–438
Ferveur JF (2005) Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav Genet 35:279–295
Finelevy JB, Derby CD (1992) Behavioral discrimination of binary mixtures and their components—effects of mixture interactions on coding of stimulus-intensity and quality. Chem Senses 17:307–323
Frambach I, Schurmann FW (2004) Separate distribution of deutocerebral projection neurons in the mushroom bodies of the cricket brain. Acta Biol Hung 55:21–29
Galizia CG, Rossler W (2010) Parallel olfactory systems in insects: anatomy and function. Annu Rev Entomol 55:399–420
Galizia CG, Szyszka P (2008) Olfactory coding in the insect brain: molecular receptive ranges, spatial and temporal coding. Entomol Exp Appl 128:81–92
Galizia CG, Nagler K, Hölldobler B, Menzel R (1998) Odour coding is bilaterally symmetrical in the antennal lobes of honeybees (Apis mellifera). Eur J Neurosci 10:2964–2974
Galizia CG, McIlwrath SL, Menzel R (1999) A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res 295:383–394
Galizia CG, Franke T, Menzel R, Sandoz JC (2012) Optical imaging of concealed brain activity using a gold mirror in honeybees. J Insect Physiol 58:743–749
Gentilcore LR, Derby CD (1998) Complex binding interactions between multicomponent mixtures and odorant receptors in the olfactory organ of the Caribbean spiny lobster Panulirus argus. Chem Senses 23:269–281
Guerenstein PG, Hildebrand JG (2008) Roles and effects of environmental carbon dioxide in insect life. Annu Rev Entomol 53:161–178
Ha TS, Smith DP (2006) A pheromone receptor mediates 11-cis-vaccenyl acetate-induced responses in Drosophila. J Neurosci 26:8728–8733
Hansson BS, Stensmyr MC (2011) Evolution of insect olfaction. Neuron 72:698–711
Hansson BS, Ochieng’ SA, Grosmaitre X, Anton S, Njagi PGN (1996) Physiological responses and central nervous projections of antennal olfactory receptor neurons in the adult desert locust, Schistocerca gregaria (Orthoptera: Acrididae). J Comp Physiol A 179:157–167
Hartlieb E, Anton S, Hansson BS (1997) Dose-dependent response characteristics of antennal lobe neurons in the male moth Agrotis segetum (Lepidoptera: Noctuidae). J Comp Physiol A 181:469–476
Heil JE, Oland LA, Lohr C (2007) Acetylcholine-mediated axon-glia signaling in the developing insect olfactory system. E J Neurosci 26:1227–1241
Heinbockel T, Kloppenburg P, Hildebrand JG (1998) Pheromone-evoked potentials and oscillations in the antennal lobes of the sphinx moth Manduca sexta. J Comp Physiol A 182:703–714
Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595–631
Hunt GJ (2007) Flight and fight: a comparative view of the neurophysiology and genetics of honey bee defensive behavior. J Insect Physiol 53:399–410
Ibba I, Angioy AM, Hansson BS, Dekker T (2010) Macroglomeruli for fruit odors change blend preference in Drosophila. Naturwissenschaften 97:1059–1066
Ignell R, Anton S, Hansson BS (2001) The antennal lobe of Orthoptera—anatomy and evolution. Brain Behav Evol 57:1–17
Ignell R, Dekker T, Ghaninia M, Hansson BS (2005) Neuronal architecture of the mosquito deutocerebrum. J Comp Neurol 493:207–240
Ito I, Bazhenov M, Ong RCY, Raman B, Stopfer M (2009) Frequency transitions in odor-evoked neural oscillations. Neuron 64:692–706
Jones CD (1998) The genetic basis of Drosophila sechellia’s resistance to a host plant toxin. Genetics 149(4):1899–1908
Kalberer NM, Reisenman CE, Hildebrand JG (2010) Male moths bearing transplanted female antennae express characteristically female behaviour and central neural activity. J Exp Biol 213:1272–1280
Karpati Z, Olsson S, Hansson B, Dekker T (2010) Inheritance of central neuroanatomy and physiology related to pheromone preference in the male European corn borer. BMC Evol Biol 10:286
Kazama H, Wilson RI (2008) Homeostatic matching and nonlinear amplification at identified central synapses. Neuron 58:401–418
Kloppenburg P, Mercer AR (2008) Serotonin modulation of moth central olfactory neurons. Annu Rev Entomol 53:179–190
Kloppenburg P, Ferns D, Mercer AR (1999) Serotonin enhances central olfactory neuron responses to female sex pheromone in the male sphinx moth Manduca sexta. J Neurosci 19:8172–8181
Kollmann M, Ninolis S, Bonhomme J, Homberg U, Schactner J, Taju D, Anton S (2011) Revisiting the anatomy of the central nervous system of a hemimetabolous model insect: the pea aphid Acyrthosiphon pisum. Cell Tissue Res 343:343–355
Kuebler LS, Olsson SB, Weniger R, Hansson BS (2011) Neuronal processing of complex mixtures establishes a unique odor representation in the moth antennal lobe. Front Neural Circuits 5:16
Kuebler LS, Schubert M, Karpati Z, Hansson BS, Olsson SB (2012) Antennal lobe processing correlates to moth olfactory behavior. J Neurosci 32:5772–5782
Laurent G (2002) Olfactory network dynamics and the coding of multidimensional signals. Nat Rev Neurosci 3:884–895
Le Conte Y, Hefetz A (2008) Primer pheromones in social hymenoptera. Ann Rev Entomol 53:523–542
Lei H, Vickers N (2008) Central processing of natural odor mixtures in insects. J Chem Ecol 34:915–927
Lei H, Christensen TA, Hildebrand JG (2002) Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons. Nat Neurosci 5:557–565
Linn C, Feder JL, Nojima S, Dambroski HR, Berlocher SH, Roelofs W (2003) Fruit odor discrimination and sympatric host race formation in Rhagoletis. Proc Natl Acad Sci USA 100:11490–11493
Linn C, Nojima S, Roelofs W (2005) Antagonist effects of non-host fruit volatiles on discrimination of host fruit by Rhagoletis flies infesting apple (Malus pumila), hawthorn (Crataegus spp.), and flowering dogwood (Cornus florida). Entomol Exp App 114:97–105
Linn CE, Yee WL, Sim SB, Cha DH, Powell THQ, Goughnour RB, Feder JL (2012) Behavioral evidence for fruit odor discrimination and sympatric host races of Rhagoletis pomonella flies in the western United States. Evolution 66:3632–3641
Linster C, Sachse S, Galizia CG (2005) Computational modeling suggests that response properties rather than spatial position determine connectivity between olfactory glomeruli. J Neurophysiol 93:3410–3417
Livermore A, Hutson M, Ngo V, Hadjisimos R, Derby CD (1997) Elemental and configural learning and the perception of odorant mixtures by the spiny lobster Panulirus argus. Physiol Behav 62:169–174
MacLeod K, Laurent G (1996) Distinct mechanisms for synchronization and temporal patterning of odor-encoding neural assemblies. Science 274:976–979
Martin JP, Beyerlein A, Dacks AM, Reisenman CE, Riffell JA, Lei H, Hildebrand JG (2011) The neurobiology of insect olfaction: sensory processing in a comparative context. Prog Neurobiol 95:427–447
Matsumoto SG, Hildebrand JG (1981) Olfactory mechanisms in the moth Manduca sexta—response characteristics and morphology of central neurons in the antennal lobe. Proc R Soc B 213:249–277
Matsuo T, Sugaya S, Yasukawa J, Aigaki T, Fuyama Y (2007) Odorant-binding proteins OBP57d and OBP57e affect taste perception and host-plant preference in Drosophila sechellia. PLoS Biol 5:e118
McPheron BA, Smith DC, Berlocher SH (1988) Genetic differences between host races of Rhagoletis pomonella. Nature 336:64–66
Meyer A, Galizia CG (2012) Elemental and configural olfactory coding by antennal lobe neurons of the honeybee (Apis mellifera). J Comp Physiol A 198:159–171
Münch D, Schmeichel B, Silbering AF, Galizia CG (2013) Weaker ligands can dominate an odor blend due to syntopic interactions. Chem Senses doi:10.1093/chemse/bjs138
Namiki S, Iwabuchi S, Kanzaki R (2008) Representation of a mixture of pheromone and host plant odor by antennal lobe projection neurons of the silkmoth Bombyx mori. J Comp Physiol A 194:501–515
Nässel DR, Winther AM (2010) Drosophila neuropeptides in regulation of physiology and behavior. Prog Neurobiol 92:42–104
Neupert S, Fusca D, Schachtner J, Kloppenburg P, Predel R (2012) Toward a single-cell-based analysis of neuropeptide expression in Periplaneta americana antennal lobe neurons. J Comp Neurol 520:694–716
Nojima S, Linn CE, Zhang A, Morris B, Roelofs WL (2003a) Identification of host fruit volatiles from hawthorn (Crataegus spp.) attractive to hawthorn-origin Rhagoletis pomonella flies. J Chem Ecol 29:319–334
Nojima S, Linn CE, Roelofs WL (2003b) Identification of host fruit volatiles from flowering dogwood (Cornus florida) attractive to dogwood-origin Rhagoletis pomonella flies. J Chem Ecol 29:2347–2357
Ochieng SA, Hallberg E, Hansson BS (1998) Fine structure and distribution of antennal sensilla of the desert locust, Schistocerca gregaria (Orthoptera: Acrididae). Cell Tissue Res 291:525–536
Ochieng SA, Park K, Baker T (2002) Host plant volatiles synergize responses of sex pheromone-specific olfactory receptor neurons in male Helicoverpa zea. J Comp Physiol A 188:325–333
Oland LA, Tolbert LP (1987) Glial patterns during early development of antennal lobe of Manduca sexta—a comparison between normal lobes and lobes deprived of antennal axon. J Comp Neurol 255:196–207
Oland LA, Tolbert LP (1996) Multiple factors shape development of olfactory glomeruli: insights from an insect model system. J Neurobiol 30:92–109
Olsen SR, Wilson RI (2008) Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452:956–960
Olsen SR, Bhandawat V, Wilson RI (2007) Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54:89–103
Olsson SB, Linn CE, Michel A, Dambroski HR, Berlocher SH, Feder JL, Roelofs WL (2006a) Receptor expression and sympatric speciation: unique olfactory receptor neuron responses in F-1 hybrid Rhagoletis populations. J Exp Biol 209:3729–3741
Olsson S, Linn CE, Roelofs WI (2006b) The chemosensory basis for behavioral divergence involved in sympatric host shifts I: characterizing olfactory receptor neuron classes responding to key host volatiles. J Comp Physiol A 192:289–300
Olsson S, Linn CE, Roelofs WI (2006c) The chemosensory basis for behavioral divergence involved in sympatric host shifts II: olfactory receptor neuron sensitivity and temporal firing pattern to key host volatiles. J Comp Physiol A 192:289–300
Party V, Hanot C, Said I, Rochat D, Renou M (2009) Plant terpenes affect intensity and temporal parameters of pheromone detection in a moth. Chem Senses 34:763–774
Peakall R (1990) Responses of male Zaspilothynnus trilobatus Turner wasps to females and the sexually deceptive orchid it pollinates. Funct Ecol 4:159–167
Perez-Orive J, Mazor O, Turner GC, Cassenaer S, Wilson RI, Laurent G (2002) Oscillations and sparsening of odor representations in the mushroom body. Science 297:359–365
Pitts RJ, Fox AN, Zwiebel LJ (2004) A highly conserved candidate chemoreceptor expressed in both olfactory and gustatory tissues in the malaria vector Anopheles gambiae. Proc Natl Acad Sci USA 101:5058–5063
Qiu YT, van Loon JJA, Takken W, Meijerink J, Smid HM (2006) Olfactory coding in antennal neurons of the malaria mosquito, Anopheles gambiae. Chem Senses 31:845–863
Raguso RA, Henzel C, Buchmann SL (2003) Trumpet flowers of the Sonoran Desert: floral biology of Peniocereus cacti and sacred Datura. Int J Plant Sci 164:877–892
Reinhard J, Sinclair M, Srinivasan MV, Claudianos C (2010) Honeybees learn odour mixtures via a selection of key odorants. PLoS ONE 5:e9110
Riffell JA (2012) Olfactory ecology and the processing of complex mixtures. Curr Opin Neurobiol 22:236–242
Riffell JA, Abrell L, Hildebrand JG (2008) Physical processes and real-time chemical measurement of the insect olfactory environment. J Chem Ecol 34:837–853
Riffell JA, Lei H, Christensen TA, Hildebrand JG (2009a) Characterization and coding of behaviorally significant odor mixtures. Curr Biol 19:335–340
Riffell JA, Lei H, Hildebrand JG (2009b) Neural correlates of behavior in the moth Manduca sexta in response to complex odors. Proc Natl Acad Sci USA 106:19219–19226
Riffell JA, Hong L, Abrell L, Hildebrand JG (2013) Neural basis of a pollinator’s buffet: olfactory specialization and learning in Manduca sexta. Science 339:200–204
Robertson HM, Wanner KW (2006) The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res 16:1395–1403
Robertson HM, Warr CG, Carlson JR (2003) Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci USA 100:14537–14542
Robertson HM, Gadau J, Wanner KW (2010) The insect chemoreceptor superfamily of the parasitoid jewel wasp Nasonia vitripennis. Insect Mol Biol 19:121–136
Roelofs WL, Liu WT, Hao GX, Jiao HM, Rooney AP, Linn CE (2002) Evolution of moth sex pheromones via ancestral genes. Proc Natl Acad Sci USA 99:13621–13626
Root CM, Semmelhack JL, Wong AM, Flores J, Wang JW (2007) Propagation of olfactory information in Drosophila. Proc Natl Acad Sci USA 104:11826–11831
Rospars JP, Chambille I (1985) Neurons and identified glomeruli of antennal lobes during postembryonic development in the cockroach Blaberus caniifer Burn (Dictyoptera: Blaberidae). Int J Insect Morphol Embryol 14:203–226
Rospars JP, Hildebrand JG (1992) Anatomical identification of glomeruli in the antennal lobes of the male sphinx moth Manduca sexta. Cell Tissue Res 270:205–227
Rössler W, Brill M (2013) Parallel processing in the honeybee olfactory pathway: structure, function and evolution. J Comp Physiol A (this issue). doi:10.1007/s00359-013-0821-y
Rössler W, Randolph PW, Tolbert LP, Hildebrand JG (1999) Axons of olfactory receptor cells of transsexually grafted antennae induce development of sexually dimorphic glomeruli in Manduca sexta. J Neurobiol 38:521–541
Rouyar A, Party V, Prešern J, Blejec A, Renou M (2011) A general odorant background affects the coding of pheromone stimulus intermittency in specialist olfactory receptor neurones. PLoS ONE 6:e26443
Sachse S, Galizia CG (2002) Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87:1106–1117
Sachse S, Galizia CG (2006) Topography and dynamics of the olfactory system. In: Grillner S, Graybiel AM (eds) Microcircuits: the interface between neurons and global brain function. Dahlem UP–MIT, Cambridge, pp 251–274
Schiestl FP, Ayasse M, Paulus HF, Löfstedt C, Hansson BS, Ibarra F, Francke W (1999) Orchid pollination by sexual swindle. Nature 399:421
Schiestl FP, Peakall R, Mant JG, Ibarra F, Schulz C, Franke S, Francke W (2003) The chemistry of sexual deception in an orchid-wasp pollination system. Science 302:437–438
Schmuker M, Schneider G (2007) Processing and classification of chemical data inspired by insect olfaction. Proc Natl Acad Sci USA 104:20285–20289
Schneiderman AM, Matsumoto SG, Hildebrand JG (1982) Trans-sexually granted antennae influence development of sexually dimorphic neurons in moth brain. Nature 298:844–846
Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23:10495–10502
Silbering AF, Galizia CG (2007) Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. J Neurosci 27:11966–11977
Silbering AF, Okada R, Ito K, Galizia CG (2008) Olfactory information processing in the Drosophila antennal lobe: anything goes? J Neurosci 28:13075–13087
Siwicki KK, Riccio P, Ladewski L, Marcillac F, Dartevelle L, Cross SA, Ferveur JF (2005) The role of cuticular pheromones in courtship conditioning of Drosophila males. Learn Memory 12:636–645
Slessor KN, Winston ML, Le Conte Y (2005) Pheromone communication in the honeybee (Apis mellifera L.). J Chem Ecol 31:2731–2745
Smid HM, Wang GH, Bukovinszky T, Steidle JLM, Bleeker MAK, Van Loon JJA, Vet LEM (2007) Species-specific acquisition and consolidation of long-term memory in parasitic wasps. Proc R Soc B 274:1539–1546
Stocker RF (1994) The organization of the chemosensory system in Drosophila melanogaster—a review. Cell Tissue Res 275:3–26
Stocker RF, Lienhard MC, Borst A, Fischbach KF (1990) Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 262:9–34
Strausfeld NJ (2012) Arthropod brains: evolution, functional elegance, and historical significance. Harvard University Press, Cambridge
Strauss K, Scharpenberg H, Crewe RM, Glahn F, Foth H, Moritz RFA (2008) The role of the queen mandibular gland pheromone in honeybees (Apis mellifera): honest signal or suppressive agent? Behav Ecol Sociobiol 62:1523–1531
Su CY, Menuz K, Carlson JR (2009) Olfactory perception: receptors, cells, and circuits. Cell 139:45–59
Su CY, Martelli C, Emonet T, Carlson JR (2011) Temporal coding of odor mixtures in an olfactory receptor neuron. Proc Natl Acad Sci USA 108:5075–5080
Su CY, Menuz K, Reisert J, Carlson JR (2012) Non-synaptic inhibition between grouped neurons in an olfactory circuit. Nature 492:66
Sun XJ, Fonta C, Masson C (1993) Odor quality processing by bee antennal lobe interneurons. Chem Senses 18:355–377
Tanaka NK, Ito K, Stopfer M (2009) Odor-evoked neural oscillations in Drosophila are mediated by widely branching interneurons. J Neurosci 29:8595–8603
Tasin M, Backman AC, Bengtsson M, Varela N, Ioriatti C, Witzgall P (2006) Wind tunnel attraction of grapevine moth females, Lobesia botrana, to natural and artificial grape odour. Chemoecol 16:87–92
Thom C, Gilley DC, Hooper J, Esch HE (2007) The scent of the waggle dance. PLoS Biol 5(9):1862–1867
Trona F, Anfora G, Bengtsson M, Witzgall P, Ignell R (2010) Coding and interaction of sex pheromone and plant volatile signals in the antennal lobe of the codling moth Cydia pomonella. J Exp Biol 213:4291–4303
Utz S, Huetteroth W, Wegener C, Kahnt J, Predel R, Schachtner J (2007) Direct peptide profiling of lateral cell groups of the antennal lobes of Manduca sexta reveals specific composition and changes in neuropeptide expression during development. Dev Neurobiol 67:764–777
van der Pers JNC, Thomas G, Denotter CJ (1980) Interactions between plant odors and pheromone reception in small ermine moths (Lepidoptera: Yponomeutidae). Chem Senses 5:367–371
Vergoz V, Schreurs HA, Mercer AR (2007) Queen pheromone blocks aversive learning in young worker bees. Science 317:384–386
Vickers NJ, Christensen TA (2003) Functional divergence of spatially conserved olfactory glomeruli in two related moth species. Chem Senses 28:325–338
Vickers NJ, Christensen TA, Baker TC, Hildebrand JG (2001) Odor-plume dynamics influence the brain’s olfactory code. Nature 410:466–470
Vickers NJ, Poole K, Linn CE (2005) Plasticity in central olfactory processing and pheromone blend discrimination following interspecies antennal imaginal disc transplantation. J Comp Neurol 491:141–156
Vosshall LB, Hansson BS (2011) A united nomenclature system for the insect olfactory coreceptor. Chem Senses 36:497–498
Vosshall LB, Stocker RE (2007) Molecular architecture of smell and taste in Drosophila. Ann Rev Neurosci 30:505–533
Wertheim B, Dicke M, Vet LEM (2002) Behavioural plasticity in support of a benefit for aggregation pheromone use in Drosophila melanogaster. Entomol Exp App 103:61–71
Wilson RI (2008) Neural and behavioral mechanisms of olfactory perception. Curr Opin Neurobiol 18:408–412
Wilson RI, Laurent G (2005) Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J Neurosci 25:9069–9079
Wilson RI, Mainen ZF (2006) Early events in olfactory processing. Ann Rev Neurosci 29:163–201
Wiltrout C, Dogra S, Linster C (2003) Configurational and nonconfigurational interactions between odorants in binary mixtures. Behav Neurosci 117:236–245
Wright GA, Lutmerding A, Dudareva N, Smith BH (2005) Intensity and the ratios of compounds in the scent of snapdragon flowers affect scent discrimination by honeybees (Apis mellifera). J Comp Physiol A 191:105–114
Wu W, Anton S, Löfstedt C, Hansson BS (1996) Discrimination among pheromone component blends by interneurons in male antennal lobes of two populations of the turnip moth, Agrotis segetum. Proc Natl Acad Sci USA 93(15):8022–8027
Yaksi E, Wilson RI (2010) Electrical coupling between olfactory glomeruli. Neuron 67:1034–1047
Yu DH, Ponomarey A, Davis RL (2004) Altered representation of the spatial code for Odors after olfactory classical conditioning: memory trace formation by synaptic recruitment. Neuron 42:437–449
Zhang QH, Schlyter F (2003) Redundancy, synergism, and active inhibitory range of non-host volatiles in reducing pheromone attraction in European spruce bark beetle Ips typographus. Oikos 101:299–310
Zhang AJ, Linn C, Wright S, Prokopv R, Reissig W, Roelofs W (1999) Identification of a new blend of apple volatiles attractive to the apple maggot, Rhagoletis pomonella. J Chem Ecol 25:1221–1232
Acknowledgments
We wish to thank J.G. Hildebrand for his mentoring and for many stimulating discussions on the mechanisms of mixture processing. K. Byers and E. Sanders provided comments that greatly improved the quality of this manuscript. Support was provided by the National Science Foundation (DBI 1121692) (JAR) and the University of Washington, Seattle, Royal Research Fund (JAR), as well as the NSF Graduate Research Fellowship (DGE-0718124; to MRC).
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Clifford, M.R., Riffell, J.A. Mixture and odorant processing in the olfactory systems of insects: a comparative perspective. J Comp Physiol A 199, 911–928 (2013). https://doi.org/10.1007/s00359-013-0818-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-013-0818-6